Anim Cogn (2006) 9:369–376 DOI 10.1007/s10071-006-0035-6
ORIGINAL ARTICLE
Pilfering ravens, Corvus corax, adjust their behaviour to social context and identity of competitors Thomas Bugnyar · Bernd Heinrich
Received: 29 August 2005 / Revised: 30 June 2006 / Accepted: 2 July 2006 / Published online: 15 August 2006 C Springer-Verlag 2006
Abstract Like other corvids, food-storing ravens protect their caches from being pilfered by conspecifics by means of aggression and by re-caching. In the wild and in captivity, potential pilferers rarely approach caches until the storers have left the cache vicinity. When storers are experimentally prevented from leaving, pilferers first search at places other than the cache sites. These behaviours raise the possibility that ravens are capable of withholding intentions and providing false information to avoid provoking the storers’ aggression for cache protection. Alternatively, birds may refrain from pilfering to avoid conflicts with dominants. Here we examined whether ravens adjust their pilfer tactics according to social context and type of competitors. We allowed birds that had witnessed a conspecific making caches to pilfer those caches either in private, together with the storer, or together with a conspecific bystander that had not created the caches (non-storer) but had seen them being made. Compared to in-private trials, ravens delayed approaching This contribution is part of the special issue “Animal Logics” (Watanabe and Huber 2006). T. Bugnyar () · B. Heinrich Department of Biology, University of Vermont, Burlington, VT 05405, USA e-mail:
[email protected] Tel.: +43-7616-8510 Fax: +43-7616-85104 B. Heinrich e-mail:
[email protected] Present address: T. Bugnyar Konrad Lorenz Research Station Gruenau and Department of Behaviour, Neurobiology, Cognition, University of Vienna, Althanstr. 14, 1090 Vienna, Austria
the caches only in the presence of storers. Furthermore, they quickly engaged in searching away from the caches when together with dominant storers but directly approached the caches when together with dominant non-storers. These findings demonstrate that ravens selectively alter their pilfer behaviour with those individuals that are likely to defend the caches (storers) and support the interpretation that they are deceptively manipulating the others’ behaviour. Keywords Raven . Corvus corax . Food caching . Deception
Introduction Social life may enhance the foraging efficiency of individuals by allowing them to exploit the knowledge of others (social learning, using public information) and/or the resources made available by others (kleptoparasitism, scrounging; review in Giraldeau and Caraco 2000; Laland 2004). Costs associated with social exploitation may be compensated by benefits through kinship or reciprocity (e.g. Axelrod and Hamilton 1981) as well as by other benefits of group living such as facilitated predator detection (e.g. Bertram 1978; Pulliam et al. 1982). However, if costs consistently exceed the benefits, individuals should develop counter-measures against exploitation, e.g. by getting away from others (Ranta et al. 1996; Barta and Giraldeau 1998) or by withholding information and providing false information (Dawkins and Krebs 1978; Maynard Smith 1979). Providing no or false information constitutes a form of deception since it leads to the misinterpretation of a situation by one individual as a consequence of the behaviour or signals of the other individual (Whiten and Byrne 1988a, b). Functionally, such a misinterpretation poses costs to the receiver Springer
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and benefits the deceiver (Semple and McComb 1996; see also Krebs and Dawkins 1984; Mitchell 1986). Byrne and Whiten (1985) introduced the term ‘tactical’ deception to emphasize a contrast between short-term tactics (in which the deception uses elements from an honest counterpart in the individuals’ repertoire) and long-term strategies such as inter- and intra-specific mimicry. Such flexible deceptive tactics for social manipulation have been reported mainly for primates (review in Byrne and Whiten 1990; Tomasello and Call 1997). Since constraints imposed by social structure (e.g. risk of detection, need for cooperation; Cheney and Seyfarth 1990a) makes deceptive tactics rare and difficult to study, much of the literature on the topic consists of anecdotes (Whiten and Byrne 1988a, b; Byrne and Whiten 1992). Nevertheless, progress in evaluating the possibility of deception has been made with experimental approaches such as the ‘informed forager’ paradigm (Menzel 1974; Coussi-Korbel 1994; Hirata and Matsuzawa 2001; Ducoing and Thierry 2003), ‘competitive experimenters’ (Woodruff and Premack 1979; Kummer et al. 1996; Mitchell and Anderson 1997; Anderson et al. 2001) or ‘food competition contest’ (Hare et al. 2000, 2001; Fujita et al. 2002), and studies have included some non-primate species (Held et al. 2000, 2002; Bugnyar and Kotrschal 2004; Dally et al. 2005a). From a cognitive perspective, tactical deception has been assumed to reflect intentions by the deceivers in the sense that individuals want to manipulate others (Whiten and Byrne 1988a, b). However, conclusions about the degree of intentionality, i.e. whether the deception aims to affect the other’s behaviour (first-order intentionality) or the other’s mental states (second-order intentionality, Dennett 1988; for a different categorization see Mitchell 1986), are speculative and therefore highly debated (e.g. open correspondence to Whiten and Byrne 1988a; Heyes 1998). Ravens are scavengers that cache temporary surpluses of food and food that is contested by others. In the wild and in captivity, they hide themselves from others while caching (Heinrich and Pepper 1998; Bugnyar and Kotrschal 2002a) in an apparent attempt to prevent conspecifics from learning about their cache locations through observation (Bugnyar and Heinrich 2003). Ravens also protect their caches against pilfering by aggressively chasing off conspecifics that come near their caches and/or by retrieving the food for later re-caching (Heinrich 1999). Thus, pilferers that have seen the making of caches often refrain from approaching those caches as long as storers are present (Bugnyar and Kotrschal 2002a). Furthermore, pilferers that are experimentally given access to the room in which they could previously observe a storer making caches, go directly for those caches when tested in private whereas they engage in short search-bouts at places away from those caches when tested together with the storer. Searching in short bouts and at various places is a typical behaviour for ravens that are ignorant about the Springer
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location of caches that they have not observed being made (Bugnyar and Heinrich 2005). These findings raise the possibility that pilferers are capable of withholding their intention and/or providing false information to avoid provoking the cache protection of storers. Alternatively, birds could delay approaching and search at places other than the caches simply to avoid conflicts with dominants. We here discriminated between these possibilities by testing whether ravens adjust their pilfer tactics according to social context and types of competitors. We gave birds who had previously watched a dominant conspecific making caches access to that room (i) in private, (ii) together with the storer, or (iii) together with a dominant conspecific that had not created the caches (non-storer) but that had observed them being made. Thus, in both social treatments, potential pilferers were confronted with dominants that were knowledgeable about cache location. However, one was the storer that was likely to retrieve caches in defence of pilfering whereas the other one was a competitor that was likely to engage in pilfering. Subordinate potential pilferers should not approach the caches when the storer is present but wait for its distraction in order to pilfer without eliciting cache protection. By contrast, if the non-storer is present then the potential pilferer should outrace its competitor because being first at the cache would be the best tactic to get the food reward against the dominant conspecific. Hence, we expected ravens to withhold pilfering and/or provide false information by searching at other places when together with storers but not with nonstorers. However, if ravens were simply avoiding conflicts with dominants, they should show those social manoeuvres with both storers and non-storers. Since ravens are known to kleptoparasite conspecifics at monopolizable food sources as well as at caches (Bugnyar and Kotrschal 2002b, 2004), both dominant storers and nonstorers could also be expected to use force to obtain the recovered cache from the focal subjects. To control for possible effects of scrounging, we used small food pieces that could be taken quickly into the beak and/or sublingual pouch (Kijne and Kotrschal 2002). Thus, in the present experiment dominants could easily use force to defend or monopolize cache sites but hardly to steal the food from others after it had been recovered.
Methods Subjects and setting Subjects were seven hand-raised ravens (five males, two females; six birds were in their first year of age, one male was in his fourth year), all of which had participated in previous studies on gaze following and food caching (Bugnyar et al. 2004; Bugnyar and Heinrich 2005). Birds were marked
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5m
St
NSt FS
Section A
Section ection B
Section C
Fig. 1 Sketch of aviary, indicating location of experimental rooms (sections B and C) and position of subjects during caching trials (St: storer; NSt: non-storer; FS: focal subject). Bold lines indicate opaque walls in section C; all other partitions between compartments were made of wire mesh
with coloured rings for individual identification. They were housed together in an outdoor aviary composed of three sections (section A: 30 m2 , section B: ca. 100 m2 , section C: three compartments and connecting pathways with a total area of 64 m2 ; Fig. 1). Sections were separated by wire partition and, in case of section C, by wooden walls containing windows that could be covered with curtains. Sections A and B were equipped with natural vegetation and diverse ground cover (trees, grass; twigs, leaves, soil) whereas compartments of section C (12 m2 , 12 m2 , and 24 m2 ) and interconnecting pathways (16 m2 ) contained only a grass-floor and a few perches. Tests were conducted in section B, potential pilferers were enclosed in section C, and birds that did not participate in a given trial were confined to section A. When experiments were not in progress, doors between compartments were open and birds could freely roam in the entire complex. Birds were fed on their normal diet (meat, milk-products, fruits; Kabicher and Fritz 1996) after daily experiments. Water was provided ad libitum. Procedure The general line of testing was the same as in Bugnyar and Heinrich (2005). Tests consisted of a caching trial and a retrieval trial for focal subjects (n = 3 trials per treatment). During caching trials, a storer received three pieces of food (meat, 10 g per piece) that it was free to cache in the entire section B. Caching trials were terminated when all food was cached (mean ± SE number of caches made per storer: 3.6 ± 0.4) and/or consumed (mean ± SE pieces recovered and consumed per storer: 1 ± 0.2) and, on average, lasted for 5( ± 0.4) min; afterwards, the storer was called out of section B by offering a small treat in the pathways of section C. During every caching trial, the focal subject and its nonstoring competitor were enclosed in section C. Each of them was in a compartment with a transparent window and/or in
the adjacent pathway from which they had clear view of the storer and the entire section B; the partition between compartments was made of wire mesh so that each bird had full visual access to the other’s room (Fig. 1). Retrieval trials started 5 min after caching trials and lasted for 10 min. During retrieval trials (n = 3 trials per treatment), focal subjects were allowed to pilfer the caches either in private or in competition with the storer and non-storer, respectively. In both social treatments, competitors were dominant to the focal subject. The order of treatments as well as the identity of competitors per treatment changed in a pseudorandomized order. In each treatment, birds were confronted with the same competitor in the first trial and, in case the birds’ position in dominance rank hierarchy allowed for more combinations, with different competitors in the second and third trial (e.g. bird with dominance status 2 was tested three times per condition with bird of dominance status 1 as storer and as non-storer; bird with dominant status 6 was tested in each condition first with bird of dominance status 5, then with birds 4 and 3). Dominance status of individuals was known before the onset of the experiments and calculated on the basis of approach-retreat interactions. Due to the size of the test compartment (section B), video-taping was inappropriate to capture the behaviour of two competitors simultaneously. Therefore, T.B. recorded all data by direct observation, marking cache locations onto pre-drawn sketches of the test compartment and describing behaviours by speaking onto a voice recorder (Olympus Pearlcorder S701). Birds were fully habituated to T.B. taking those types of protocols from a given point outside the aviary which was a standard procedure executed since fledging for 1–3 h per day. During caching trials, he recorded the location of caches, the order in which they were made and the number of immediate recoveries by the storer (see above). During retrieval trials, he measured the number and location of searches by the focal subject (labelled as searchbouts), the time (s) spent searching and the total time elapsed until the first cache was approached
